Newly modified ‘pseudo flap’ without compromising vascularity to enhance repair of long distal ureteral loss: A retrospective analysis of a prospective database

Abstract Objective To present an alternative technique called pseudo‐flap for reconstructing long ureteral defects as an alternative to Boari flap. Despite being used for more than 70 years by urologists for tension‐free reconstruction of distal and mid‐ureteral defects, the Boari flap exhibits high complication rates, with an average of 27% (range 5.5%–30.4%). These complications arise from compromised blood supply, attributed to incisions made on all three sides of the flap and dependence on the flap base as the sole source of blood supply. Methods We retrospectively reviewed patients who underwent our modified technique by a single surgeon between 2008 and 2021. We used a semi‐oblique cystotomy on the lowest part of the anterior and contralateral aspects of the bladder after complete release from adhesions and sacrificing the superior vesical pedicle, if necessary. The innovative part of the technique involved making short relaxing incisions at different levels on both sides of a pseudo‐flap while pushing the bladder dome upward to reach the healthy ureter in a tension‐free manner, followed by anastomosis with a non‐refluxing or refluxing technique. Results Fifteen patients underwent the pseudo‐flap technique with a mean follow‐up of 16.9 months. Four had prior radiation, three had hyperthermic intraperitoneal chemotherapy (HIPEC) for peritoneal carcinomatosis, and one had a ureteral stricture in a transplanted kidney. Eight procedures were performed during intraoperative consultations. Only one patient (7%) developed a major complication (Clavien–Dindo grade ≥2). This patient developed postoperative leak, and none developed obstructive hydronephrosis, suggesting stricture or flap ischemia. The mean length of the flap was 9.3 cm. Conclusion Our pseudo‐flap technique has lower complication rates than the traditional Boari flap. It is not technically challenging, minimally compromises blood supply and is thus especially suitable for complex, highly morbid patients with decreased tissue vascularity, such as those with prior radiation and peritoneal carcinomatosis.

and is thus especially suitable for complex, highly morbid patients with decreased tissue vascularity, such as those with prior radiation and peritoneal carcinomatosis.Based on the multitude of primary aetiologies, the length and the location of the ureteric loss, management of ureteral injuries can be a dilemma.Because longer and more proximal ureteral segments cannot be merely repaired with end-to-end anastomosis or ureteral reimplant without considerable tension, many other methods for reconstruction have been explained.Techniques for repairing ureteral injuries are numerous and versatile, including direct ureteral reimplant into the bladder dome, ureteroureterostomy, psoas hitch, Boari flap, autologous grafts, 1 ileal interposition, 2 transureteroureterostomy, 3 bridging the gap with appendix or ovarian tube and on-lay flap with buccal or lingual mucosa; all have been described with different success rates.
Bladder flap was first described by the Italian Urologist Achille Boari in 1894 in canine models, 4 and even before that by Van Hook in cadavers. 5This technique was implemented in patients for the first time in 1963 by Ockerblad. 6,7The Boari flap, or ureteroneocystostomy using a raised bladder flap, is still widely used by urologists for the reconstruction of ureteric injuries in both longer segments 8 and further locations up to mid and proximal ureter, 9 with relatively favourable outcomes in long-term follow-up.Despite the versatility of its indications and common use in urological surgeries, there is currently scarce literature considering the outcomes and complications of the Boari flap procedure. 10,11Complications, mostly anastomotic stricture and leakage, can arise from the technique itself in which incision is made on three sides of the flap and blood supply is exclusively driven from the flap's base.Other reasons for complications are various patient risk factors, such as previous radiation exposure, active cancer and unsuccessful prior procedures.These factors interfere with the proper blood supply and healing process, ultimately leading to a higher rate of failure.Management of complications after the Boari flap is usually very challenging and includes re-doing Boari flaps 11 ileal ureter, new techniques for ureteral grafts 12 or permanent stents or nephrostomy tubes and nephrectomy as the last resort.
To prevent complications of the Boari flap, especially stricture formation, we developed a pseudo-flap technique, which is a modification of previous procedures.We have been applying it to all patients who potentially need the Boari flap in the past several years.
Our technique, invented by the senior author, is a modification of the psoas hitch technique, described by Turner-Warwick. 13In his psoas hitch technique, Turner-Warwick was making a few centimetres long, oblique incision in the lowest part of the bladder on the contralateral side of the flap and pushing the bladder dome upward from inside to elevate the bladder dome in the ipsilateral side, where it can be hitched to the psoas muscle.Unfortunately, the length acquired by this method, on many occasions, is not long enough.The short releasing incisions in both sides, wherever the flap is under tension, increase the length of the pseudo-flap significantly without compromising its blood supply.This is contrary to the Boari flap technique in which incisions in three different sides of the flap leave the flap solely dependent on its base for blood supply.Here, we aim to describe the pseudo-flap technique and retrospectively review the outcomes in our very complicated population of patients who underwent our modified technique and compare these outcomes with reported series in the literature.

| MATERIALS AND METHODS
We retrospectively reviewed medical charts of all patients who underwent our modified technique in the Department of Urology at Wake Forest School of Medicine performed by a single surgeon from 2008 to 2018.Our cohort were consecutive patients, with our inclusion criteria being whenever ureteral reimplantation with traditional Boari flap or psoas hitch has not been possible and another method of ureteral reconstruction had to be resorted to.As a salvage technique, the exclusion criteria for this procedure are limited to cases where easier alternatives such as reimplantation with a traditional Boari flap or psoas hitch were feasible.
Patient demographics and characteristics are summarized in Table 1.The cohort is generally typical of highly complex patients, which we define as a patient population in which ureteric reimplantation using conventional methods to replace ureteral loss would generally have a higher risk of failure.This complex patient condition can result from various conditions that affect tissue vascularity, and thus later viability of flaps used in reconstruction, as previous history of malignancy, radiation, chemotherapy and so forth.
Follow-up visits after surgery were performed at 3 months, 12 months and then annually.The patient's symptoms, voiding history, post-void residual urine and renal ultrasound were performed during each visit.Many patients with cancer history had multiple imaging in between for surveillance of their cancers.Failure of the flap was defined as postoperative leak or obstructive hydronephrosis, which would suggest flap ischemia or stricture reformation.

| Surgical technique
In the supine position, a low midline incision is made to expose the normal ureter, which is then dissected down to the fibrotic ureter.To aid in the orientation of the distal ureter during anastomosis and prevent rotation, a marking suture is passed at the 12 o'clock position.Next, the most distal part of the healthy ureter is clipped and cut.The bladder is filled with 300 mL of saline, and the distance between the normal ureter and the bladder is measured.This measurement determines the extent of dissection on the contralateral side of the bladder.
The anterior surface of the bladder down to the bladder neck is dissected and freed.The ligation of the superior vesical pedicle on the contralateral side is optional and mainly dependent on the length of the gap.
A curvilinear incision of 5 cm is made in the lowest part of the anterior surface on the contralateral side (Figure 1A).Using a finger in the bladder dome area, we attempt to reach the uppermost part of the bladder to the healthy ureter (Figure 2).If the gap is long, we detect tethering points in the bladder wall, which prevent complete bridging of the gap, by pushing the bladder toward the ureter.We make a 5-mm releasing incision on one side in a tethering point, and then, if needed, another 5-mm incision on the opposite side a few millimetres higher.If more length is needed, then another set of incisions is made 1-2 cm above the previous ones.This process of The cystostomy is performed by making an approximately 5-cm curvilinear incision in the anterior surface of the contralateral side of the bladder after dissecting and freeing the anterior surface of the bladder down to the bladder neck.(B & C) While attempting to reach the bladder flap to the most distal part of the healthy ureter, we detect a tethering point and make a 5-mm incision on one side at this exact point and another 5-mm incision on the opposite side.Another set of incisions is made 1-2 cm above the previous ones to eventually reach the bladder to the normal ureter without tension.
F I G U R E 2 The surgeon's finger is inserted in the bladder dome area in an attempt to reach the uppermost part of the bladder to the healthy ureter.If the gap between the bladder and the most distal part of the healthy ureter is long, we make sets of oppositely situated 5-mm incisions on both sides of our bladder flap to bridge the gap without tension.BMI in kg/m 2 , mean (range) 27.9 (16.7-50.9)

Comorbid conditions
Prior transplant procedures, n (%) 1 ( 7) HIPEC patients with peritoneal carcinomatosis, n Prior radiation history, n (%) 4 ( 27 After performing the stented anastomosis, the pseudo-flap is secured to the psoas minor tendon using two 2/0 PDS sutures.At this point, the pseudo-flap is tabularized.Once tabularization is complete, the pseudo-flap appears as a fully tabularized flap, and the rest of the bladder is repaired in two layers using 2/0 Vicryl stitches.A Foley catheter remains in place for 2-3 weeks and is removed after a cystogram (Figure 3) shows no signs of leakage.A drain is left in, and the patient is discharged the following day.

| RESULTS
We utilized the pseudo-flap technique in a total of 15 patients between 2008 and 2018.Among the patients, four were male and 11 were female.Their ages ranged from 29 to 89 years, with a mean age of 58.5 years.The mean body mass index (BMI) was 27.9 kg/m 2 , ranging from 16.7 to 50.9.In eight out of the 15 cases, intraoperative consultations were performed without preoperative planning.Two of these consultations were for hysterectomy patients, and the other six were for surgeries related to non-genitourinary malignancies treated with hyperthermic intraperitoneal chemotherapy (HIPEC).The remaining seven patients underwent elective procedures, consisting of five surgeries for native ureteral strictures, one for a stricture in a transplanted ureter and one for a ureteral defect resulting from urothelial cancer in the distal ureter.
Among the patients, eight (53%) had comorbid conditions: Four patients (27%) had prior radiation, three (20%) underwent concomitant HIPEC for peritoneal carcinomatosis during the surgery and one (7%) required repair of a transplant ureteral stricture.The remaining seven patients did not have any preoperative confounding issues.In our cohort, the mean length of the ureteral defect was 9.3 cm, ranging from 3 to 16 cm.This is also the final length of the pseudo-flap obtained by the multiple small incisions done in our technique.We measured the gap from the distal part of the healthy ureter to the dome of the bladder; the real ureteral defect was significantly longer.
There is no specified width of the flap because we did not make an were reserved for patients who developed de novo hydronephrosis after surgery, which did not occur in our patients.The Clavien-Dindo grading system 14 was used for reporting postoperative complications.
In the follow-up period, one patient (7%) developed postoperative leak (Clavien-Dindo grade 3), a complication not uncommon following ureteric reimplantation according to the EAU guidelines panel assessment, and was appropriately managed with nephrostomy 15 that was removed later and did not develop complications on long-term followup.None of our patients developed obstructive hydronephrosis (Clavien-Dindo grade 2-3), suggesting anastomotic stricture or flap ischemia.Moreover, none of our patients experienced urinary retention, severe frequency, urgency or urinary incontinence (Clavien-Dindo grade 1) after surgery.These findings are consistent with the literature, indicating that bladder function remains independent of its configuration, and the bladder retains its functionality even after reconfiguration.Considering our highly complex patient population, characterized by long ureteric stricture lengths (mean of 9.3 cm) and a lengthy follow-up period (mean of 16.9 months), we believe that our modification demonstrates reliability and yields favourable outcomes.
Our approach exhibits lower complication rates compared with the traditional Boari flap technique and is suitable for complex patients with compromised tissue vascularity resulting from factors such as previous surgeries, concomitant chemotherapy, radiation or renal transplantation.
F I G U R E 3 This is a cystogram done 2 weeks after using the bladder pseudo-flap to replace a lost ureteric segment.The cystogram shows an intact pseudo-flap with no leakage and thus a successful repair.At this point, the Foley catheter can be removed.
Repairing long ureteral strictures has always presented a challenge, leading to the development of numerous techniques for this purpose.
These methods range from straightforward approaches like direct ureteroureterostomy and ureteroneocystostomy to more complex techniques such as psoas hitch, Boari flap, transureteroureteral anastomosis, autologous grafts from oral mucosae (buccal and lingual mucosae), urogenital mucosae (renal pelvis wall, penile/preputial skin and vein), ureteral replacement with appendix or ileum and potential future options like ureteral tissue engineering, 1 as well as renal autotransplantation.
The Boari flap has been widely used as a method of ureteroneocystostomy for bridging longer segments of the ureter. 8,9However, there is limited literature available on surgical outcomes associated with this technique. 10,11Reported complications include urinary leak, uroperitoneum (Clavien-Dindo grade ≥2) and uretero-vaginal and uretero-enteric fistula (Clavien-Dindo grade ≥3), as well as late complications such as anastomotic strictures with recurrent hydronephrosis (Clavien-Dindo grade ≥3), which may require permanent stents, nephrostomy tubes or even nephrectomy. 10,11,16rious authors have documented their experiences with the Boari flap technique, providing insights into outcomes, success rates and complication rates.In Table 2, we have compiled a comprehensive list of the most relevant papers in this regard.The authors argued that this modification enables direct finger insertion into the bladder, facilitating its fixation to the ipsilateral psoas tendon.This modification appears to have a positive impact on flap vascularity, viability and the overall surgical field.In their cohort of 24 patients, the authors reported no instances of chronic flank pain, recurrent pyelonephritis, persistent severe hydronephrosis, compromised renal function or the need for reoperation due to complications or repair failure during the follow-up period. 28Our technique represents a further modification of this approach, with the short relaxing incisions at different levels on both sides of the pseudoflap and the mobilization of the bladder dome upward providing extra length to reach the healthy ureter in a tension-free manner.
Other authors have attempted to completely abandon the Boari flap and instead utilized onlay flaps from buccal or lingual mucosa, along with other techniques, to address long segments of the ureter. 1 Unfortunately, most of the studies in the literature discussing outcomes of the Boari flap or alternative procedures are not without flaws: 1.These studies often report combined outcome results for various approaches, including the Boari flap, to repair ureteral injuries.
They generally do not specify the proportion of failures associated with a specific procedure, making it impossible to determine the specific outcomes of the Boari flap (Wenske et al., 26 Helfland et al., 25 Gozen et al., 24 Matthew et al., 17 Brian W Chao et al., 18 Riedmiller et al. 23 ).
2. The follow-up periods vary significantly among the studies.Some have short follow-up durations.
3. Most of these studies consist of small case series, such as Ben Sionov et al., 11 Yucai Wu et al., 12 Alsaadi et al., 20 Farzad et al. 21d AbdelBakayko et al. 22 4.The length of the ureteric segment has not been mentioned in many reports, including those by Ben Sionov et al., 11 Wenske et al., 26 Gozen et al. 24 and AbdelBakayko et al. 22 All of these limitations make it exceedingly challenging to make an objective assessment of the success of the Boari flap procedure based on the available literature.It is also imperative to note that accurately establishing the precise complication rates attributable to the specific utilization of the Boari flap is challenging because most studies reported complication rates collectively for all techniques employed for ureteral reconstruction.Nonetheless following the Boari flap, based on our literature review, the occurrence rate of major postoperative complications (Clavien-Dindo grade ≥2), namely anastomotic leak or ureteral stricture yielding obstructive hydronephrosis with or without subsequent renal impairment, is high, with an average of approximately 27% (ranging from 5.5% to 30.4%).This high complication rate may result from incisions made on three sides of the flap, relying solely on the flap base for blood supply and increasing the risk of subsequent flap ischemia.In our approach, we avoid making incisions on all three sides, resulting in improved blood supply.Our series demonstrates a lower incidence rate (7%) of these complications (ureteral stricture and anastomotic leak) compared with the average rate (27%) reported in the reviewed literature.Based on our findings, we believe that our pseudo-flap technique serves as a viable alternative to the Boari flap, yielding improved outcomes compared to the series reported in the literature.However, it is important to acknowledge that the generalizability of our results may be limited because of the nature of this case series, which was conducted by a single surgeon on a small number of patients.Additionally, the follow-up period was relatively short for some patients, primarily because of mortality resulting from underlying comorbidities.
We acknowledge that our group of patients is non-homogenous with different underlying diseases that may interfere with the interpretation of the outcome.However, being applicable in patients having a wide variety of conditions with good outcomes is the hallmark of our proposed surgical technique.Therefore, further research is urgently needed to explore the application of this innovative technique on a larger scale, involving multiple institutions and a larger patient cohort.
Furthermore, although all of our patients underwent open surgery, it appears feasible to adapt this surgical technique to laparoscopic or robotic approaches, applying the same principles.

| CONCLUSION
We recommend utilizing the 'pseudo-flap' modification as a replacement for the Boari flap technique.This modification is supported by a solid anatomical foundation, offers favourable long-term outcomes, can be applied to highly morbid patients with extensive ureteral injuries and is not overly complex from a technical standpoint.However, to establish this procedure as a standard technique for repairing long lower defects in the lower and mid portions of the ureter, further studies involving a larger patient cohort and multiple surgeons are necessary in the future.

AUTHOR CONTRIBUTIONS
Dr Mirzazadeh developed the modified surgical technique.
Dr Whitney Smith gathered data retrospectively from patients' charts who underwent the newly devised technique over 10 years.
Dr Badran was responsible for writing the manuscript besides doing a review of reports that found drawbacks to the traditional Boari flap and/or developed alternative methods of ureteral reimplantation.

K
E Y W O R D S Boari, pseudo-flap, psoas hitch, ureteric injury, ureteroureterostomy 1 | INTRODUCTION Ureteral injuries have always been challenging to the surgical team.
incision around it.Furthermore, the diameter of the pseudo-flap is dependent on the number of small incisions made, with more incisions resulting in a longer flap and smaller diameter.The mean follow-up period for our patients was 16.9 months, ranging from 1 to 60 months.Except for one patient, all patients had at least 6 months of follow-up.This patient had a follow-up only at 1 month but could not make it to the second follow-up and died because of complications from widespread cancer.Our follow-up protocol included a voiding trial and measurement of residual urine at the time of Foley catheter removal, which occurred 2-3 weeks after surgery.Stent removal visits were scheduled for 4-6 weeks after surgery.Subsequent follow-up visits were performed at 3 months, 12 months and then annually.During each visit, we assessed the patient's symptoms, voiding history and post-void residual urine and conducted a renal ultrasound.Patients with a history of cancer often had multiple imaging sessions in between visits for cancer surveillance.Renal scans In a study conducted by Kunj Jain et al. in 2022, the authors examined 50 patients who underwent ureteral reimplantation with the Boari flap and reported an 88% success rate, with six documented cases of failure.Surgical 'failure' was defined as the presence of flank pain or imaging evidence of ureteral obstruction, the need for or presence of hardware despite undertaking the procedure or the requirement for repeated ureteral reconstruction.10In a report byBenson et al. in 1990, the authors shared their experience with ureteric reimplantation in 18 cases, six of which have undergone psoas hitches and Boari flaps.They reported an overall success rate of 94%.In the psoas hitch/Boari flap group, one out of six patients (17%) experienced failure of the ureteral reconstruction.The patient developed subsequent hydronephrosis and cortical atrophy (Clavien-Dindo grade 2 or 3a), which were managed with ureteral stents.9This report is advantageous as it attributes complications specifically to the method of ureteral reconstruction used, providing valuable insights into the potential drawbacks of each approach.Because of the limitations associated with the traditional Boari flap, the necessity for modifications or alternatives has emerged.Several reports have highlighted new or modified techniques.In 2001, Ahn et al. introduced a modified psoas hitch ureteral reimplantation technique that avoids extending the bladder cystostomy to the dome.